Journal of Pollination Ecology, 27(5), 2021, pp 57-64
POLLINATION OF NYPA FRUTICANS (WURMB.) IN A SOUTH FLORIDA BOTANIC GARDEN
Imeña R. Valdes1-4, Joanna M. Tucker Lima1, Larry R. Noblick1 1Montgomery Botanical Center, 11901 Old Cutler Road, Coral Gables, FL 33156 USA 2Department of Biological Sciences, Florida International University, Miami, FL 33199 USA 3Program in Plant Biology and Conservation, Northwestern University, 633 Clark Street, Evanston, IL 60208 4Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, IL 60022 USA
Abstract—When plants are removed from their native habitat, reproduction can be compromised if pollinators are absent, especially when plant-pollinator interactions are species-specific and the plant is self-incompatible. To avoid these pitfalls, botanic gardens often use hand pollination to ensure reproductive success of their living collections, an important aspect of ex-situ conservation. The nipa palm, Nypa fruticans, presents an interesting case study of pollination in a botanic garden and a plant’s ability to successfully reproduce outside its native range without assisted pollination. Nypa fruticans has been growing at Montgomery Botanical Center (MBC) in South Florida since 1984, but for years required hand pollination to produce viable fruit. A recent shift from hand pollination to unassisted pollination suggests that this palm has found an alternative to fertilize its flowers. We investigate possible pollinators and new opportunities for pollination outside the palm’s native range. Rather than the insects typically associated with N. fruticans pollination in its native range in Southeast Asia (i.e., flies and beetles), ants, specifically Paratrechina longicornis, were overwhelmingly the most abundant visitors to nipa palm inflorescences at MBC and likely represent an important pollinator or facilitator of pollination at the garden. Pollination research at botanic gardens complements in-situ field studies and provides important insights into the flexibility of pollination systems to achieve reproductive success outside a plant’s native range. Keywords: Nypa fruticans, plant-animal interactions, nipa palm, ant pollination, mangrove, phenology
INTRODUCTION circumstances, exotic plants can successfully establish within natural plant communities, although sometimes to the Introduced exotic plants are not always able to reproduce detriment of local plant species (Sunderland & Morakinyo outside their native range unless they are self-compatible or 2002). Although the current literature on reproductive act as generalist species able to attract new pollinators from biology of exotic plant populations provides insights into the local area (Thompson & Knight 2018). Plants that rely on pollinator limitation and facilitation of exotic and naturalized specialized pollinators from their native habitat may be less plant populations, information regarding pollination of exotic integrated into exotic plant-pollinator networks, limiting non-naturalized plants, such as those found at botanic gardens successful reproduction outside their native range (Memmot and arboreta, is scarce (Thompson & Knight 2018). & Waser 2002; Thompson & Knight 2018); however, if a plant is served well by generalist pollinators, then it will likely Successful fruit production by plants grown in botanic overcome these obstacles (Memmot & Waser 2002). The gardens and arboreta is never guaranteed, but oftentimes the more generalized the pollinator, the more exotic plants it mission of such gardens involves advancing ex-situ includes in its diet (Memmot & Waser 2002). Razanajatovo conservation through seed production. To overcome the et al. (2015) suggest that plant species unable to maintain self- absence of native pollinators, gardens sometimes rely on hand sustaining populations may be pollinator limited. Across pollination to ensure successful reproduction, thus Europe, invasive plants living among natives were frequently maintaining seed production for distribution and storage to found to be visited by local native pollinators, and these conserve genetic resources for future generations. At pollinators often came to rely more on the invasive plants than Montgomery Botanical Center (MBC) in South Florida, the natives (Vilà et al. 2009). Sargent and Ackerly (2008) garden staff hand pollinate multiple rare and endangered claim that plants in small, isolated populations have the most species, including several cycad species (i.e., Cycas to gain from living among other plants that attract similar micronesica, Microcycas calocoma, Zamia lucayana) and tree pollinators, dubbed pollinator facilitation. Under these species, like Brownea capitella (Fabaceae). Nypa fruticans Wurmb. (Arecaceae), the mangrove palm commonly known as the nipa palm, is no exception. This species is native to Southeast Asia and grows mainly in brackish coastal areas. Received 04 July 2020, accepted 21 March 2021 First planted at MBC in 1984, the garden’s nipa palms *Corresponding author: [email protected] represent the only known healthy collection of this species growing in North America. For years, successful fruit set
57 58 VALDES ET AL. J Poll Ecol 27(5) required careful hand pollination, but in 2008 MBC scientists Nypa fruticans grows at four locations on MBC property, observed the first open-pollinated nipa fruits (Noblick et al. but thus far, successful fruit set has only been reported at two 2018). Shortly thereafter, a major freeze in 2010 destroyed all sites (Fig. 1). The garden palms were grown from seed developing nipa inflorescences, but with time N. fruticans collected in Malaysia and Indonesia in 1984 and 1998, recovered. Hand pollinations resumed for a number of years, respectively. The nipa palm has large pinnate leaves and a but the practice was discontinued in 2016. From 2017 subterranean stem with dichotomous branching and is onward, open-pollinated, viable nipa fruits have again been monoecious, displaying distinct male and female structures observed (Noblick et al. 2018). Has a mystery pollinator from within the same inflorescence (Fig. 1B; Uhl 1972). South Florida assumed the role of pollinator in N. fruticans? Nipa flowering is protogynous with the first male rachillae Have the nipa palms at MBC resorted to self-pollination to beginning to open a day after the onset of female anthesis successfully reproduce? In this study, we investigate the (Mantiquilla et al. 2013). Multiple male spikes on each reproductive biology of N. fruticans grown in a botanic inflorescence open in succession over the next several days and garden setting in South Florida, in order to identify the produce large amounts of pollen. Nipa palms rely on insects mysterious pollinator/s and discover how this palm species for pollination (Essig 1973; Mantiquilla et al. 2016), as the has been able to produce viable fruits without human spikey pollen grains are both sticky and heavy, making wind intervention after several years of dependence on hand transport highly unlikely (Fig. 2). During receptivity, pollination. stigmatic fluid is present on the three separate carpels that make up each female flower and are arranged in a tight, single MATERIALS AND METHODS head (Fig. 1B). Fruits mature over several months into a large, Study Site & Species Description heavy globular head (Fig. 1C), which may become so heavy in the wild that it topples into the water, where it breaks apart Montgomery Botanical Center (MBC; Coral Gables, into individual floating fruits that disperse and establish Florida, USA) is a research garden in South Florida that themselves at new locations. focuses on palms, cycads, and tropical conifers. The climate is humid and subtropical, and over the past 20 years the area Nypa fruitcans phenology experienced an average annual temperature of 25.3⁰C and Montgomery Botanical Center monthly phenology average annual rainfall of 1698 mm (NOAA 2020), having records from 1994–1997 were consulted to assess time of wet summers and dry winters. flowering. In addition, five inflorescences on two different Nypa fruticans is one of only two palms known to live plants were observed daily in 2018 for the duration of male and grow with their trunk submerged underwater; the other and female anthesis, and photographic images were taken to being Ravenea musicalis from Madagascar. The nipa palm is characterize the flowering cycle from pre-anthesis through native to estuarine mangrove vegetation and can be found in senescence. Each inflorescence was assigned a designated ID India and Sri Lanka, throughout Southeast Asia, and as far as (i.e., A, B, C, D, E). Both the male and female parts are bright Northern Australia. In the early 1900s, N. fruticans was yellow orange when they emerge, and fade to a white or tan introduced to Nigeria and has since spread and become color, respectively, over time. To characterize the invasive along the western coast of Africa (Numbere 2019; developmental stages of the inflorescence, we used color and Moudingo et al. 2020). Additional reports of established woodiness for the female phase, and we visually accessed the populations in areas of the Caribbean, including Trinidad, amount of pollen for the male phase based on color and Panama and Guyana, further attest to nipa’s ability to thrive coverage of the anthers. outside its native range (Noblick et al. 2018).
FIGURE 1. Nypa fruticans at Montgomery Botanical Center (MBC) in Coral Gables, Florida: (A) healthy stand of N. fruticans planted in 1984 and 1999, (B) recently opened N. fruticans inflorescence showing both the pistillate (female) flower head and newly opened staminate (male) flower spikes, and (C) developing N. fruticans infructescence head.
April 2021 POLLINATION OF NYPA FRUTICANS IN SOUTH FLORIDA 59
of approximately two feet from the center of the inflorescence. We documented insect visitors by functional group (i.e., fly, bee, beetle, ant, etc.) and noted any other identifying features. In all, we recorded approximately 47.75 hours of observations. During collection times, insects that were seen interacting with the reproductive parts of the male and/or female flowers were collected using a vial aspirator with various 7.62 cm plastic tubes for storing the insects. During each collection, we divided insects into multiple plastic tubes for space and to avoid any negative interactions that could harm the sample. Overall, we spent 42.5 hours in the field collecting insects. Collected insects were identified by experts at Florida International University and the University of Florida/Florida Department of Agriculture and Consumer Services. RESULTS
Flowering phenology Monthly phenology records gathered at Montgomery Botanical Center between 1994 and 1997 indicate peak nipa flowering occurs during wetter summer months. We observed very few inflorescences during the dry/colder winter months in South Florida (January-March). Palms that were wild collected as seed from Malaysia began their flowering cycle two months before those from Indonesia. At MBC, the female flower head emerges 1–2 days before any male flower spikes appear (Fig. 3). During these first days, FIGURE 2. Scanning Electron Microscopic images of Nypa the female flowers secrete clear stigmatic fluid, indicating fruticans pollen collected at Montgomery Botanical Center in Coral receptivity (Straarup et al. 2018). By the fourth day after the Gables, Florida. pistillate head emerges, the stigmatic fluid begins to dry out, signaling the end of female receptivity and within eight days Pollinator Observations & Insect Collections the flower head hardens into a woody mass of distinct carpels We determined insect visitors to Nypa fruticans through (Fig. 3). Approximately three days after the female flowers field observations and insect collections on the two nipa palms appear, multiple bracts containing male flower spikes open noted to have successfully reproduced without hand and more continue to emerge over the next several days. The pollination. Between April and July 2018, we monitored five male flower spikes show highest pollen loads during the first distinct inflorescences: A, B, C, D, and E. Both A and B 2–3 days after emerging from their peduncular bracts, underwent unstructured pollinator observations and appearing bright yellow orange in color, and exuding a strong collections. Inflorescences C and D followed a tight protocol pungently sweet smell. Beginning on the third day, flower to balance time between observations and collections, and petals turn progressively beige, while the anthers and pollen inflorescence E was observed but no insect collections were fade to an off-white color (Fig. 3). carried out. Insect Visitors Due to a brief overlap in receptivity between the female Four functional groups of insects were recorded during and male anthesis within the same inflorescence (ca. one day), pollinator observations with ants being the most frequently we alternated pollinator observations and insect collection observed (N = 156) (Fig. 4, Fig. 5). Flies were the second times on sequential days for inflorescences C and D (e.g., most often observed insect (N = 54), while bees (N = 7) and Monday: morning observations, afternoon collections; beetles (N = 2) were rarely seen (Fig. 4, Fig. 5). Insect Tuesday: morning collections, afternoon observations; collections corroborated our observations, revealing a greater Wednesday: morning observations, afternoon collections; presence of ants (N = 50) than any other functional group of etc.). Morning was defined as any consecutive two-hour insects. Otherwise, three flies, one planthopper (Fig. 4B), and period between 7:00 AM and 11:00 AM, while in the one bee (Fig. 4C) were collected from the nipa inflorescences afternoon we recorded insects during a consecutive two-hour (Tab. 1). period between 12:00 PM and 4:00 PM. The dominant visitor observed on female flowers was the For each observation, we recorded the date, start and end ant: 91% of observed insect visitors (N = 51). The only other times, temperature (⁰C), and general weather conditions. We insects observed on the female flower head were flies (N = 6). closely observed both the female and male flowers at a distance Visitors observed on male rachillae were more diverse, with
60 VALDES ET AL. J Poll Ecol 27(5)
FIGURE 3. Nypa fruticans inflorescence development through female (top row) and male (bottom row) anthesis, captured at Montgomery Botanical Center in Coral Gables, Florida.
the majority of visitors being flies (68%; N = 40), followed by ants (17%; N = 10), bees (12%; N = 7) and beetles (3%; N = 2). Only ants and flies were observed on both female and male flower structures. In addition to the ants observed on each sex individually, 30 more were observed crossing between male rachillae and female head, and we were able to track one fly as it travelled between female and male flowers. We found no clear differences in insect visitation between AM and PM observations, although it should be noted that when combined, our data exhibited an unintentional skew toward morning observations and collections for all inflorescences except A. During observations and collections, temperature varied between 21–32⁰C. Flower visitation rates showed no clear patterns associated with temperature–neither for insect visitors overall, nor for the distinct functional groups. We observed and collected the more common visitors (ants and flies) throughout the temperature range. Ants & Nypa fruticans Our pollinator observations and insect collections revealed an abundance of Paratrechina longicornis, commonly known as the crazy ant. They are common to the tropics and not generally recognized as pollinators (but see Takahashi et al. 1993). Crazy ants were seen walking between female and male inflorescences, sometimes carrying eggs, and at other times they appeared to be eating pollen or drinking the stigmatic fluid from receptive parts of the female flowers. We observed clumps of pollen grains on the exterior of the ants’ bodies, clearly visible to the naked eye and could see ant mandibles moving but could not confirm that they were consuming pollen.
DISCUSSION Pollination and successful fruit set of non-native plant species conserved in botanic gardens and arboreta present intriguing questions that remain poorly understood. In ex-situ conservation, curators often rely on hand pollination to ensure
purity of offspring and help guard against the reproductive FIGURE 4. Insects observed on Nypa fruticans (A) failure in non-anemophilous species growing outside their Paratrechina longicornis tending a scale, (B) Bothriocera sp., (C) Apis native range. Within the context of botanic gardens, many mellifera on male, (D) unknown beetle on male, (E) unknown fly on conspecifics with distinct native ranges thrive together in one male, and (F) two Paratrechina longicornis near male inflorescence. place, and pollen limitation often compromises successful
April 2021 POLLINATION OF NYPA FRUTICANS IN SOUTH FLORIDA 61
TABLE 1. Total counts of observed and collected insect visitors to Nypa fruticans growing at Montgomery Botanical Center in Coral Gables, Florida.
Insect Functional Total Insects Total Insects Species name* Order Family Group Observed Collected ant 156 50 Paratrechina Hymenoptera Formicidae longicornis (Latreille) fly 54 4 Drosophila sp., subgenus Diptera Drosophilidae and Sophophora and Unknown unknown bee 7 1 Apis mellifera Linnaeus Hymenoptera Apidae
beetle 2 0 Typhaea stercorea (Linnaeus) Coleoptera Mycetophagidae and and Anthocoridae Anthocoridae planthopper 0 1 Bothriocera sp. Hemiptera Cixiidae
elevated pollen availability–enough for local pollinators to show an interest in this species, thus surmounting issues of pollen limitation (Burd 1994). Alternatively, autogamy is theoretically possible due to the brief overlap in male and female anthesis within the same inflorescence. Similar to our findings, Mantiquilla et al. (2018) reported that stigma receptivity peaks at 12 h after anthesis and significantly declines after 48 h completing the cycle within 72 h. At MBC, male flower spikes begin opening the second and third day after the female flower head emerges, making self-fertilization theoretically possible. The possibility of wind pollination is unlikely. Nipa pollen is sticky and heavy (Essig 1973). Furthermore, the position of the male rachillae, generally to the sides and beneath the female flower head, reduces the chance that pollen will fall onto receptive female flowers. These characteristics suggest N. fruticans is not adapted for anemophily as a primary mode of pollen transfer, but rather point to entomophily as the principal means to reproduction. Studies from its native range in Southeast Asia highlight beetles, weevils, flies, and bees as potential pollinators of N. fruticans (Essig 1973; Tan 2008; Mantiquilla et al. 2016; Panabang et al. 2017; Straarup et al. 2018). To our surprise, these native pollinator groups were extremely rare on nipa inflorescences in the garden. Ant visitors greatly outnumbered beetles, flies, and bees observed on nipa inflorescences at MBC. FIGURE 5. Female (L) and male (R) inflorescences of Nypa A key detail in confirming an insect’s role as pollinator is fruticans with (A, B) Paratrechina longicornis and (C, D) Drosophila activity on both male and female flowers. Without this sp. overlap, insect visitors are largely inconsequential. We frequently witnessed ants traveling between male and female fruit production. For this reason, successful N. fruticans fruit flowers. Flies also visited both male and female inflorescences, set after hand pollination stopped at MBC is particularly although they preferred male flowers. Only a single fly was interesting. Not only are the palms growing outside of their observed flying between male and female flower branches, but native range, far from native pollinators, they have no the difficulty of following flying insects after they take flight conspecifics with which to hybridize. This species has either may explain this low rate of observation. Since bees and beetles been exposed to local insects that fill the role of pollinator, or were only observed or collected on male flowers, we assume self-fertilization has found success in these palms after a they play no significant role in nipa pollination at MBC. period of adaptation. The oldest nipa palms at MBC, planted in 1984, have been flowering for the past 25 years. A recent While ants were clearly the most abundant visitors to the uptick in inflorescence production as younger specimens, nipa flowers at MBC, until recently their role as pollinator has planted in 1999 and 2000, matured may have triggered been downplayed in the scientific literature. Ants produce an
62 VALDES ET AL. J Poll Ecol 27(5) antimicrobial secretion that can reduce pollen viability (Beattie the female nipa head warms up to six degrees Celsius above et al. 1985), and this negative role in pollination has been ambient temperature before opening (Straarup et al. 2018). widely assumed to be the norm until recently, as a growing This attracts insects, particularly ovipositing beetles, as number of studies have demonstrated effective pollination by warmth promotes egg and larvae development (Barfod et al. ant species in some plants (Hickman 1974; Rostás & Tautz 2011). The inflorescence also serves as an ideal breeding and 2011; De Vega & Gomez 2014; Domingos-Melo et al. 2017; brood site for insects due to the many layers of bracts that Delnevo et al. 2020). The ant species found on our nipa envelop its inflorescence structures (Panabang et al. 2017). palms, Paratrechina longicornis, is widespread in the U.S. and Weevils were mostly found inside inflorescence bracts, but does not appear to be a newcomer to South Florida. Other they also visited flowers of both sexes. Panabang et al. (2017) nipa studies reported the presence of ants but discarded them also observed pollen-covered sap beetles visiting the pistillate as potential pollinators. In Thailand, Hoppe (2005) observed head of nipa inflorescences and noted that smaller sap beetle ants on nipa flowers during anthesis but assumed they play species and weevils have an advantage in pollination as they only a minor role in self-pollination. In the Philippines, are small enough to crawl into the locular canals of the female Panabang et al. (2017) observed ants on nipa pistillate heads, flower head, facilitating pollination. At MBC, we collected feeding on gelatinous stigmatic secretions, but attributed their neither sap beetles, nor weevils. Instead, we encountered beetle presence to aphids that serve as a source of honeydew. At species from the Mycetophagidae and Anthocoridae families. MBC, we also observed ants tending to aphids on nipa This was somewhat surprising, since Nitidulidae and inflorescences (Fig. 4A). In Thailand, Straarup et al. (2018) Curculionidae are widely distributed throughout South regularly observed “patrolling ants” on nipa inflorescences, Florida (Parsons 1943; Giblin-Davis et al. 1996). presumably collecting stigmatic fluid from female flowers, but In spite of nipa’s dependence on insect pollinators in their unlike our study, these same ants rarely visited male rachillae native range, self-compatibility cannot be excluded (Straarup during female anthesis. If ants are indeed the nipa pollinator et al. 2018). Hoppe (2005) found no fruit set in three we are looking for at MBC, our study represents one of the inflorescences bagged as part of his pollinator exclusion rare cases where an ant acts as pollinator, and the first reported experiment. Mantiquilla et al. (2016), on the other hand, instance of ant pollination in a species outside its native range. reported 50% fruiting success from self-pollination in Since travel between different inflorescences is highly unlikely Philippine nipa populations, but with a caveat: loosely tied with nipa inflorescences often blooming at least several meters pollinator exclusion bags may have unintentionally permitted apart, the ants’ role may be restricted to facilitating self- the entrance of pollinators. Preliminary results at MBC pollination rather than effecting cross-pollination. If nipa indicate successful self-pollination in at least two of three palms are relying on ants for pollination, and consequently inflorescences bagged for pollinator exclusion (unpublished self-pollination dominates, then inbreeding depression might data) and raises the question as to whether mature fruits found help explain the low success rate of fully developed fruits per at the garden resulted from self-pollination. Even so, this fails female inflorescence head that we observed at MBC (cf. to explain why successful fruit set has only occurred within Rostás et al. 2018). the last decade. A likely explanation is an increase in flowering In Nypa fruticans, stigmatic fluid on the receptive carpels frequencies and pollen availability as our N. fruticans of the female flower head attracts insects (Hoppe 2005), collections have matured, coupled with the introduction of a along with a distinct floral scent, which is intensified by the new pollinator to the area, or heightened interest from local heat of thermogenesis. The floral scent chemistry for N. pollinators that have either facilitated self-pollination or fruticans contains compounds that are highly attractive for played an active role in cross-pollination. Overall, fruit set Scarab beetles (Scarabaeidae) and some flies (Azuma et al. remains low but persistent for open pollinated N. fruticans at 2002). Flies were the second most common visitor to nipa at MBC. Nipa palms at MBC produce more failed MBC, yet their abundance paled in comparison to the number infructescences (with aborted fruit) than mature of ants recorded. Within nipa’s native range, flies are infructescences, and even the successful infructescences usually repeatedly cited as potential pollinators (Essig 1973, bear only a handful of viable fruits per head. This suggests Mantiquilla et al. 2016, Panabang et al. 2017). Diptera were reduced success rates due to selfing (Mantiquilla et al. 2013), the most abundant insects (48%) in Philippines’ nipa stands, or pollen limitation. Molecular analyses of our nipa palms and followed by Coleoptera (beetles; 22%) (Panabang et al. their offspring would help clarify these unknowns. Whether 2017). Panabang et al. (2017) observed Musca sp. flies laying it is self- or cross-pollination, one thing is certain: open eggs on nipa inflorescence bracts and Drosophila spp. feeding pollinated nipa flowers are now producing viable seed. on pollen and stigmatic fluid. Essig (1973) observed Due to their large numbers and visitation to both male and drosophilid flies on both male and female nipa flowers in female flowers, ants are likely to be contributing to pollination Papua New Guinea and found that nipa inflorescences of N. fruticans at MBC. Inflorescence architecture and the provide a burrowing-feeding site for fly larvae, and when adult timing of the male and female phases strongly favors cross- flies emerge, their pollen-covered bodies carry pollen to other pollination by minimizing chances for self-pollination, but inflorescences. Mantiquilla et al. (2016), also identified both pollinators with a restricted foraging range, such as ants, could drosophilid flies and nitidulid beetles as likely pollinators of be facilitating self-pollination (Peakall & Beattie 1991; nipa flowers in the Philippines. Panabang et al. (2017) and Gomez & Zamora 1992; De Vega et al. 2009), albeit at a low Straarup et al. (2018) agree that nitidulids (sap beetles) and success rate. Pollination research in botanic gardens curculionids (weevils) play a key role in N. fruticans complements field studies and provides insight into flexibility pollination across their native range. During thermogenesis,
April 2021 POLLINATION OF NYPA FRUTICANS IN SOUTH FLORIDA 63 of reproduction outside of a species’ native range, producing Mantiquilla JA, Abad RG, Barro KMG, Basilio JAM, Rivero GC, valuable information for ex-situ conservation efforts. Silvosa CSC (2016) Potential pollinators of nipa palm (Nypa fruticans Wurmb.). Asia Life Sciences 25:435-474. ACKNOWLEDGEMENTS Mantiquilla JA, Ponce KCB, Concepcion KC, Rivero GC, Millado CSS, Abad RG (2018) Infructescence development and fruit Many thanks to Chad Evans and Julian Lentz for assisting with characterization of nipa (Nypa fruticans Wurmb.) from the semi- field work and to the staff at Montgomery Botanical Center for wild stands of the Davao Region, Philippines. Banwa B. 13:art013. logistical support. Dr. Gary Steck, Dr. Susan Halbert, and Dr. Memmot J, Waser NM (2002) Integration of alien plants into a Suzanne Koptur for their entomological expertise. We would like to native flower–pollinator visitation web. 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